The Functions of the Microbiome in Skin Health and Disease

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Medical Microbiology".

Deadline for manuscript submissions: closed (30 June 2019) | Viewed by 88153

Special Issue Editors

School of Biological Sciences, Queen's University, Belfast BT9 7AE, UK
Interests: Propionibacterium acnes; bacteriophage; probiotics; acne vulgaris; skin microbiome
Northern Ireland Centre for Stratified Medicine, University of Ulster, Londonderry BT47 6SB, UK
Interests: medical microbiology; bacterial pathogens; gram positive; propionibacteria; acne; medical device infection; genome sequencing; sequence analysis; bacterial evolution; molecular systematics; bacterial taxonomy; phylogenetics; genetic population analysis; typing; MLST

Special Issue Information

Dear Colleagues,

The skin plays an important role in protecting the body from invasion of foreign materials and harmful pathogens. One of the mechanisms by which the skin can perform this role is through the activities and interactions of the resident bacterial, fungal, and viral species. Commensal microbes are essential to skin health but, on occasion, the same microorganism conferring a health benefit can also lead to a diseased state when their abundances and activities change or when the environmental conditions become less favorable as a result of alterations in the host. In this Special Issue, we highlight the roles of beneficial skin organisms in protecting against colonization and infection of pathogens, guiding the host immune system, and discuss their functional changes and interactions with the host in response to environmental changes.

Dr. Emma Barnard
Dr. Andrew McDowell
Guest Editors

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Keywords

  • skin microbiome
  • propionibacteria
  • staphylococci
  • bacteriophage
  • skin probiotics
  • acne
  • atopic dermatitis
  • psoriasis
  • skin health
  • cosmetics

Published Papers (8 papers)

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Research

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14 pages, 1367 KiB  
Article
MG-MLST: Characterizing the Microbiome at the Strain Level in Metagenomic Data
by Nathanael J. Bangayan, Baochen Shi, Jerry Trinh, Emma Barnard, Gabriela Kasimatis, Emily Curd and Huiying Li
Microorganisms 2020, 8(5), 684; https://doi.org/10.3390/microorganisms8050684 - 08 May 2020
Cited by 8 | Viewed by 4208
Abstract
The microbiome plays an important role in human physiology. The composition of the human microbiome has been described at the phylum, class, genus, and species levels, however, it is largely unknown at the strain level. The importance of strain-level differences in microbial communities [...] Read more.
The microbiome plays an important role in human physiology. The composition of the human microbiome has been described at the phylum, class, genus, and species levels, however, it is largely unknown at the strain level. The importance of strain-level differences in microbial communities has been increasingly recognized in understanding disease associations. Current methods for identifying strain populations often require deep metagenomic sequencing and a comprehensive set of reference genomes. In this study, we developed a method, metagenomic multi-locus sequence typing (MG-MLST), to determine strain-level composition in a microbial community by combining high-throughput sequencing with multi-locus sequence typing (MLST). We used a commensal bacterium, Propionibacterium acnes, as an example to test the ability of MG-MLST in identifying the strain composition. Using simulated communities, MG-MLST accurately predicted the strain populations in all samples. We further validated the method using MLST gene amplicon libraries and metagenomic shotgun sequencing data of clinical skin samples. MG-MLST yielded consistent results of the strain composition to those obtained from nearly full-length 16S rRNA clone libraries and metagenomic shotgun sequencing analysis. When comparing strain-level differences between acne and healthy skin microbiomes, we demonstrated that strains of RT2/6 were highly associated with healthy skin, consistent with previous findings. In summary, MG-MLST provides a quantitative analysis of the strain populations in the microbiome with diversity and richness. It can be applied to microbiome studies to reveal strain-level differences between groups, which are critical in many microorganism-related diseases. Full article
(This article belongs to the Special Issue The Functions of the Microbiome in Skin Health and Disease)
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12 pages, 1873 KiB  
Article
5-Methyl Furfural Reduces the Production of Malodors by Inhibiting Sodium l-Lactate Fermentation of Staphylococcus epidermidis: Implication for Deodorants Targeting the Fermenting Skin Microbiome
by Manish Kumar, Binderiya Myagmardoloonjin, Sunita Keshari, Indira Putri Negari and Chun-Ming Huang
Microorganisms 2019, 7(8), 239; https://doi.org/10.3390/microorganisms7080239 - 05 Aug 2019
Cited by 8 | Viewed by 4679
Abstract
Staphylococcus epidermidis (S. epidermidis) is a common bacterial colonizer on the surface of human skin. Lactate is a natural constituent of skin. Here, we reveal that S. epidermidis used sodium l-lactate as a carbon source to undergo fermentation and yield [...] Read more.
Staphylococcus epidermidis (S. epidermidis) is a common bacterial colonizer on the surface of human skin. Lactate is a natural constituent of skin. Here, we reveal that S. epidermidis used sodium l-lactate as a carbon source to undergo fermentation and yield malodors detected by gas colorimetric tubes. Several furan compounds such as furfural originating from the fermentation metabolites play a role in the negative feedback regulation of the fermentation process. The 5-methyl furfural (5MF), a furfural analog, was selected as an inhibitor of sodium l-lactate fermentation of S. epidermidis via inhibition of acetolactate synthase (ALS). S. epidermidis treated with 5MF lost its ability to produce malodors, demonstrating the feasibility of using 5MF as an ingredient in deodorants targeting malodor-causing bacteria in the skin microbiome. Full article
(This article belongs to the Special Issue The Functions of the Microbiome in Skin Health and Disease)
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4657 KiB  
Article
The Skin Bacterium Propionibacterium acnes Employs Two Variants of Hyaluronate Lyase with Distinct Properties
by Seven Nazipi, Kristian Stødkilde, Carsten Scavenius and Holger Brüggemann
Microorganisms 2017, 5(3), 57; https://doi.org/10.3390/microorganisms5030057 - 12 Sep 2017
Cited by 36 | Viewed by 12580
Abstract
Hyaluronic acid (HA) and other glycosaminoglycans are extracellular matrix components in the human epidermis and dermis. One of the most prevalent skin microorganisms, Propionibacterium acnes, possesses HA-degrading activity, possibly conferred by the enzyme hyaluronate lyase (HYL). In this study, we identified the [...] Read more.
Hyaluronic acid (HA) and other glycosaminoglycans are extracellular matrix components in the human epidermis and dermis. One of the most prevalent skin microorganisms, Propionibacterium acnes, possesses HA-degrading activity, possibly conferred by the enzyme hyaluronate lyase (HYL). In this study, we identified the HYL of P. acnes and investigated the genotypic and phenotypic characteristics. Investigations include the generation of a P. acnes hyl knockout mutant and HYL activity assays to determine the substrate range and formed products. We found that P. acnes employs two distinct variants of HYL. One variant, HYL-IB/II, is highly active, resulting in complete HA degradation; it is present in strains of the phylotypes IB and II. The other variant, HYL-IA, has low activity, resulting in incomplete HA degradation; it is present in type IA strains. Our findings could explain some of the observed differences between P. acnes phylotype IA and IB/II strains. Whereas type IA strains are primarily found on the skin surface and associated with acne vulgaris, type IB/II strains are more often associated with soft and deep tissue infections, which would require elaborate tissue invasion strategies, possibly accomplished by a highly active HYL-IB/II. Full article
(This article belongs to the Special Issue The Functions of the Microbiome in Skin Health and Disease)
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Review

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19 pages, 295 KiB  
Review
The Skin and Gut Microbiome and Its Role in Common Dermatologic Conditions
by Samantha R. Ellis, Mimi Nguyen, Alexandra R. Vaughn, Manisha Notay, Waqas A. Burney, Simran Sandhu and Raja K. Sivamani
Microorganisms 2019, 7(11), 550; https://doi.org/10.3390/microorganisms7110550 - 11 Nov 2019
Cited by 98 | Viewed by 19916
Abstract
Microorganisms inhabit various areas of the body, including the gut and skin, and are important in maintaining homeostasis. Changes to the normal microflora due to genetic or environmental factors can contribute to the development of various disease states. In this review, we will [...] Read more.
Microorganisms inhabit various areas of the body, including the gut and skin, and are important in maintaining homeostasis. Changes to the normal microflora due to genetic or environmental factors can contribute to the development of various disease states. In this review, we will discuss the relationship between the gut and skin microbiome and various dermatological diseases including acne, psoriasis, rosacea, and atopic dermatitis. In addition, we will discuss the impact of treatment on the microbiome and the role of probiotics. Full article
(This article belongs to the Special Issue The Functions of the Microbiome in Skin Health and Disease)
22 pages, 1395 KiB  
Review
Staphylococcus aureus and the Cutaneous Microbiota Biofilms in the Pathogenesis of Atopic Dermatitis
by Enea Gino Di Domenico, Ilaria Cavallo, Bruno Capitanio, Fiorentina Ascenzioni, Fulvia Pimpinelli, Aldo Morrone and Fabrizio Ensoli
Microorganisms 2019, 7(9), 301; https://doi.org/10.3390/microorganisms7090301 - 29 Aug 2019
Cited by 62 | Viewed by 8656
Abstract
Biofilm is the dominant mode of growth of the skin microbiota, which promotes adhesion and persistence in the cutaneous microenvironment, thus contributing to the epidermal barrier function and local immune modulation. In turn, the local immune microenvironment plays a part in shaping the [...] Read more.
Biofilm is the dominant mode of growth of the skin microbiota, which promotes adhesion and persistence in the cutaneous microenvironment, thus contributing to the epidermal barrier function and local immune modulation. In turn, the local immune microenvironment plays a part in shaping the skin microbiota composition. Atopic dermatitis (AD) is an immune disorder characterized by a marked dysbiosis, with a sharp decline of microbial diversity. During AD flares biofilm-growing Staphylococcus aureus emerges as the major colonizer in the skin lesions, in strict association with disease severity. The chronic production of inflammatory cytokines in the skin of AD individuals concurs at supporting S. aureus biofilm overgrowth at the expense of other microbial commensals, subverting the composition of the healthy skin microbiome. The close relationship between the host and microbial biofilm resident in the skin has profound implications on human health, making skin microbiota an attractive target for the therapeutic management of different skin disorders. Full article
(This article belongs to the Special Issue The Functions of the Microbiome in Skin Health and Disease)
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17 pages, 603 KiB  
Review
Microbiota and Immune-Mediated Skin Diseases—An Overview
by Adrian Catinean, Maria Adriana Neag, Andrei Otto Mitre, Corina Ioana Bocsan and Anca Dana Buzoianu
Microorganisms 2019, 7(9), 279; https://doi.org/10.3390/microorganisms7090279 - 21 Aug 2019
Cited by 24 | Viewed by 5046
Abstract
In recent years, increased attention has been paid to the relationship between microbiota and various diseases, especially immune-mediated diseases. Because conventional therapy for many autoimmune diseases is limited both in efficacy and safety, there is an increased interest in identifying nutraceuticals, particularly probiotics, [...] Read more.
In recent years, increased attention has been paid to the relationship between microbiota and various diseases, especially immune-mediated diseases. Because conventional therapy for many autoimmune diseases is limited both in efficacy and safety, there is an increased interest in identifying nutraceuticals, particularly probiotics, able to modulate the microbiota and ameliorate these diseases. In this review, we analyzed the research focused on the role of gut microbiota and skin in immunity, their role in immune-mediated skin diseases (IMSDs), and the beneficial effect of probiotics in patients with this pathology. We selected articles published between 2009 and 2019 in PubMed and ScienceDirect that provided information regarding microbiota, IMSDs and the role of probiotics in these diseases. We included results from different types of studies including observational and interventional clinical trials or in vivo and in vitro experimental studies. Our results showed that probiotics have a beneficial effect in changing the microbiota of patients with IMSDs; they also influence disease progression. Further studies are needed to better understand the impact of new therapies on intestinal microbiota. It is also important to determine whether the microbiota of patients with autoimmune diseases can be manipulated in order to restore homeostasis of the microbiota. Full article
(This article belongs to the Special Issue The Functions of the Microbiome in Skin Health and Disease)
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29 pages, 3687 KiB  
Review
Propionibacterium acnes and Acne Vulgaris: New Insights from the Integration of Population Genetic, Multi-Omic, Biochemical and Host-Microbe Studies
by Joseph McLaughlin, Steven Watterson, Alison M. Layton, Anthony J. Bjourson, Emma Barnard and Andrew McDowell
Microorganisms 2019, 7(5), 128; https://doi.org/10.3390/microorganisms7050128 - 13 May 2019
Cited by 107 | Viewed by 16086
Abstract
The anaerobic bacterium Propionibacterium acnes is believed to play an important role in the pathophysiology of the common skin disease acne vulgaris. Over the last 10 years our understanding of the taxonomic and intraspecies diversity of this bacterium has increased tremendously, and with [...] Read more.
The anaerobic bacterium Propionibacterium acnes is believed to play an important role in the pathophysiology of the common skin disease acne vulgaris. Over the last 10 years our understanding of the taxonomic and intraspecies diversity of this bacterium has increased tremendously, and with it the realisation that particular strains are associated with skin health while others appear related to disease. This extensive review will cover our current knowledge regarding the association of P. acnes phylogroups, clonal complexes and sequence types with acne vulgaris based on multilocus sequence typing of isolates, and direct ribotyping of the P. acnes strain population in skin microbiome samples based on 16S rDNA metagenomic data. We will also consider how multi-omic and biochemical studies have facilitated our understanding of P. acnes pathogenicity and interactions with the host, thus providing insights into why certain lineages appear to have a heightened capacity to contribute to acne vulgaris development, while others are positively associated with skin health. We conclude with a discussion of new therapeutic strategies that are currently under investigation for acne vulgaris, including vaccination, and consider the potential of these treatments to also perturb beneficial lineages of P. acnes on the skin. Full article
(This article belongs to the Special Issue The Functions of the Microbiome in Skin Health and Disease)
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3242 KiB  
Review
Over a Decade of recA and tly Gene Sequence Typing of the Skin Bacterium Propionibacterium acnes: What Have We Learnt?
by Andrew McDowell
Microorganisms 2018, 6(1), 1; https://doi.org/10.3390/microorganisms6010001 - 21 Dec 2017
Cited by 30 | Viewed by 16238
Abstract
The Gram-positive, anaerobic bacterium Propionibacterium acnes forms part of the normal microbiota on human skin and mucosal surfaces. While normally associated with skin health, P. acnes is also an opportunistic pathogen linked with a range of human infections and clinical conditions. Over the [...] Read more.
The Gram-positive, anaerobic bacterium Propionibacterium acnes forms part of the normal microbiota on human skin and mucosal surfaces. While normally associated with skin health, P. acnes is also an opportunistic pathogen linked with a range of human infections and clinical conditions. Over the last decade, our knowledge of the intraspecies phylogenetics and taxonomy of this bacterium has increased tremendously due to the introduction of DNA typing schemes based on single and multiple gene loci, as well as whole genomes. Furthermore, this work has led to the identification of specific lineages associated with skin health and human disease. In this review we will look back at the introduction of DNA sequence typing of P. acnes based on recA and tly loci, and then describe how these methods provided a basic understanding of the population genetic structure of the bacterium, and even helped characterize the grapevine-associated lineage of P. acnes, known as P. acnes type Zappe, which appears to have undergone a host switch from humans-to-plants. Particular limitations of recA and tly sequence typing will also be presented, as well as a detailed discussion of more recent, higher resolution, DNA-based methods to type P. acnes and investigate its evolutionary history in greater detail. Full article
(This article belongs to the Special Issue The Functions of the Microbiome in Skin Health and Disease)
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